P4 ATPases - The physiological relevance of lipid flipping transporters

FEBS Letters

Volumn 584, Issue 13, 2010, Pages 2708-2716

  Paulusma, Coen C ^a   Oude Elferink, Ronald P J ^a  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

Cholesterol; Flippase; Lipid asymmetry; Phospholipid; Vesicular transport

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CHAPERONE; LIPID; P4 ADENOSINE TRIPHOSPHATASE; PHOSPHOLIPID; PROTEIN ALA1; PROTEIN ALA2; PROTEIN ALA3; PROTEIN ATP10A; PROTEIN ATP8A1; PROTEIN ATP8A2; PROTEIN ATP8B1; PROTEIN ATP8B3; PROTEIN ATP8B4; PROTEIN CDC50; PROTEIN DRS2P; PROTEIN TAT1; PROTEIN TAT2; PROTEIN TAT4; SECRETORY PROTEIN; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG;

ARABIDOPSIS; BIOGENESIS; CAENORHABDITIS ELEGANS; CELL FUNCTION; CELL VACUOLE; ENDOCYTOSIS; ENZYME ACTIVITY; ENZYME BINDING; ENZYME INACTIVATION; ENZYME REGULATION; ENZYME SUBSTRATE; HUMAN; INTRACELLULAR TRANSPORT; MAMMAL CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOSPHOLIPID TRANSFER; PHYLOGENY; PRIORITY JOURNAL; PROTEIN DEFECT; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN LIPID INTERACTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; REVIEW; SACCHAROMYCES CEREVISIAE;

ADENOSINE TRIPHOSPHATASES; ANIMALS; BIOLOGICAL TRANSPORT; CHOLESTEROL; HUMANS; MEMBRANE TRANSPORT PROTEINS; PHOSPHOLIPIDS; PHYLOGENY; SACCHAROMYCES CEREVISIAE; TRANSPORT VESICLES;

MAMMALIA; SACCHAROMYCES CEREVISIAE;

EID: 77953725368     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2010.04.071     Document Type: Review

References (110)

1. Bretscher M.S. Asymmetrical lipid bilayer structure for biological membranes. Nat. New Biol. 1972, 236:11-12.
2. Gordesky S.E., Marinetti G.V. The asymetric arrangement of phospholipids in the human erythrocyte membrane. Biochem. Biophys. Res. Commun. 1973, 50:1027-1031.
3. Verkleij A.J., Zwaal R.F., Roelofsen B., Comfurius P., Kastelijn D., van Deenen L.L. The asymmetric distribution of phospholipids in the human red cell membrane. A combined study using phospholipases and freeze-etch electron microscopy. Biochim. Biophys. Acta 1973, 323:178-193.
4. Butikofer P., Lin Z.W., Chiu D.T., Lubin B., Kuypers F.A. Transbilayer distribution and mobility of phosphatidylinositol in human red blood cells. J. Biol. Chem. 1990, 265:16035-16038.
5. Gascard P., Tran D., Sauvage M., Sulpice J.C., Fukami K., Takenawa T., Claret M., Giraud F. Asymmetric distribution of phosphoinositides and phosphatidic acid in the human erythrocyte membrane. Biochim. Biophys. Acta 1991, 1069:27-36.
6. Low M.G., Finean J.B. Modification of erythrocyte membranes by a purified phosphatidylinositol-specific phospholipase C (Staphylococcus aureus). Biochem. J. 1977, 162:235-240.
7. Sprong H., van der Sluijs P., van Meer G. How proteins move lipids and lipids move proteins. Nat. Rev. Mol. Cell Biol. 2001, 2:504-513.
8. Balasubramanian K., Schroit A.J. Aminophospholipid asymmetry: a matter of life and death. Annu. Rev. Physiol. 2003, 65:701-734.
9. Zwaal R.F., Comfurius P., Bevers E.M. Surface exposure of phosphatidylserine in pathological cells. Cell Mol. Life Sci. 2005, 62:971-988.
10. Lee A.G. How lipids affect the activities of integral membrane proteins. Biochim. Biophys. Acta 2004, 1666:62-87.
11. Devaux P.F., Lopez-Montero I., Bryde S. Proteins involved in lipid translocation in eukaryotic cells. Chem. Phys. Lipids 2006, 141:119-132.
12. Holthuis J.C., Levine T.P. Lipid traffic: floppy drives and a superhighway. Nat. Rev. Mol. Cell Biol. 2005, 6:209-220.
13. van Meer G., Halter D., Sprong H., Somerharju P., Egmond M.R. ABC lipid transporters: extruders, flippases, or flopless activators?. FEBS Lett. 2006, 580:1171-1177.
14. Seigneuret M., Devaux P.F. ATP-dependent asymmetric distribution of spin-labeled phospholipids in the erythrocyte membrane: relation to shape changes. Proc. Natl. Acad. Sci. USA 1984, 81:3751-3755.
15. Zachowski A., Henry J.P., Devaux P.F. Control of transmembrane lipid asymmetry in chromaffin granules by an ATP-dependent protein. Nature 1989, 340:75-76.
16. Tang X., Halleck M.S., Schlegel R.A., Williamson P. A subfamily of P-type ATPases with aminophospholipid transporting activity. Science 1996, 272:1495-1497.
17. Halleck M.S., Lawler J.F., Blackshaw S., Gao L., Nagarajan P., Hacker C., Pyle S., Newman J.T., Nakanishi Y., Ando H., et al. Differential expression of putative transbilayer amphipath transporters. Physiol. Genomics 1999, 1:139-150.
18. Paulusma C.C., Oude Elferink R.P. The type 4 subfamily of P-type ATPases, putative aminophospholipid translocases with a role in human disease. Biochim. Biophys. Acta 2005, 1741:11-24.
19. Folmer D.E., Elferink R.P., Paulusma C.C. P4 ATPases - lipid flippases and their role in disease. Biochim. Biophys. Acta 2009, 1791:628-635.
20. Muthusamy B.P., Natarajan P., Zhou X., Graham T.R. Linking phospholipid flippases to vesicle-mediated protein transport. Biochim. Biophys. Acta 2009, 1791:612-619.
21. Gall W.E., Geething N.C., Hua Z., Ingram M.F., Liu K., Chen S.I., Graham T.R. Drs2p-dependent formation of exocytic clathrin-coated vesicles in vivo. Curr. Biol. 2002, 12:1623-1627.
22. Hua Z., Fatheddin P., Graham T.R. An essential subfamily of Drs2p-related P-type ATPases is required for protein trafficking between Golgi complex and endosomal/vacuolar system. Mol. Biol. Cell 2002, 13:3162-3177.
23. Liu K., Surendhran K., Nothwehr S.F., Graham T.R. P4-ATPase requirement for AP-1/clathrin function in protein transport from the trans-Golgi network and early endosomes. Mol. Biol. Cell 2008, 19:3526-3535.
24. Furuta N., Fujimura-Kamada K., Saito K., Yamamoto T., Tanaka K. Endocytic recycling in yeast is regulated by putative phospholipid translocases and the Ypt31p/32p-Rcy1p pathway. Mol. Biol. Cell 2007, 18:295-312.
25. Liu K., Hua Z., Nepute J.A., Graham T.R. Yeast P4-ATPases Drs2p and Dnf1p are essential cargos of the NPFXD/Sla1p endocytic pathway. Mol. Biol. Cell 2007, 18:487-500.
26. Sakane H., Yamamoto T., Tanaka K. The functional relationship between the Cdc50p-Drs2p putative aminophospholipid translocase and the Arf GAP Gcs1p in vesicle formation in the retrieval pathway from yeast early endosomes to the TGN. Cell Struct. Funct. 2006, 31:87-108.
27. Chantalat S., Park S.K., Hua Z., Liu K., Gobin R., Peyroche A., Rambourg A., Graham T.R., Jackson C.L. The Arf activator Gea2p and the P-type ATPase Drs2p interact at the Golgi in Saccharomyces cerevisiae. J. Cell Sci. 2004, 117:711-722.
28. Natarajan P., Liu K., Patil D.V., Sciorra V.A., Jackson C.L., Graham T.R. Regulation of a Golgi flippase by phosphoinositides and an ArfGEF. Nat. Cell Biol. 2009, 11:1421-1426.
29. Puts C.F., Lenoir G., Krijgsveld J., Williamson P., Holthuis J.C. A P(4)-ATPase protein interaction network reveals a link between aminophospholipid transport and phosphoinositide metabolism. J. Proteome Res. 2009.
30. Vicinanza M., D'Angelo G., Di C.A., De Matteis M.A. Function and dysfunction of the PI system in membrane trafficking. EMBO J. 2008, 27:2457-2470.
31. Wang Y.J., Wang J., Sun H.Q., Martinez M., Sun Y.X., Macia E., Kirchhausen T., Albanesi J.P., Roth M.G., Yin H.L. Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi. Cell 2003, 114:299-310.
32. Alder-Baerens N., Lisman Q., Luong L., Pomorski T., Holthuis J.C. Loss of P4 ATPases Drs2p and Dnf3p disrupts aminophospholipid transport and asymmetry in yeast post-Golgi secretory vesicles. Mol. Biol. Cell 2006, 17:1632-1642.
33. Natarajan P., Wang J., Hua Z., Graham T.R. Drs2p-coupled aminophospholipid translocase activity in yeast Golgi membranes and relationship to in vivo function. Proc. Natl. Acad. Sci. USA 2004, 101:10614-10619.
34. Chen S., Wang J., Muthusamy B.P., Liu K., Zare S., Andersen R.J., Graham T.R. Roles for the Drs2p-Cdc50p complex in protein transport and phosphatidylserine asymmetry of the yeast plasma membrane. Traffic 2006, 7:1503-1517.
35. Zhou X., Graham T.R. Reconstitution of phospholipid translocase activity with purified Drs2p, a type-IV P-type ATPase from budding yeast. Proc. Natl. Acad. Sci. USA 2009, 106:16586-16591.
36. Pomorski T., Lombardi R., Riezman H., Devaux P.F., van Meer G., Holthuis J.C. Drs2p-related P-type ATPases Dnf1p and Dnf2p are required for phospholipid translocation across the yeast plasma membrane and serve a role in endocytosis. Mol. Biol. Cell 2003, 14:1240-1254.
37. Riekhof W.R., Voelker D.R. Uptake and utilization of lyso-phosphatidylethanolamine by Saccharomyces cerevisiae. J. Biol. Chem. 2006, 281:36588-36596.
38. Riekhof W.R., Wu J., Gijon M.A., Zarini S., Murphy R.C., Voelker D.R. Lysophosphatidylcholine metabolism in Saccharomyces cerevisiae: the role of P-type ATPases in transport and a broad specificity acyltransferase in acylation. J. Biol. Chem. 2007, 282:36853-36861.
39. Hua Z., Graham T.R. Requirement for neo1p in retrograde transport from the Golgi complex to the endoplasmic reticulum. Mol. Biol. Cell 2003, 14:4971-4983.
40. Wicky S., Schwarz H., Singer-Kruger B. Molecular interactions of yeast Neo1p, an essential member of the Drs2 family of aminophospholipid translocases, and its role in membrane trafficking within the endomembrane system. Mol. Cell Biol. 2004, 24:7402-7418.
41. Prezant T.R., Chaltraw W.E., Fischel-Ghodsian N. Identification of an overexpressed yeast gene which prevents aminoglycoside toxicity. Microbiology 1996, 142(Pt 12):3407-3414.
42. Goodyear R.J., Gale J.E., Ranatunga K.M., Kros C.J., Richardson G.P. Aminoglycoside-induced phosphatidylserine externalization in sensory hair cells is regionally restricted, rapid, and reversible. J. Neurosci. 2008, 28:9939-9952.
43. Hasson T. Myosin VI: two distinct roles in endocytosis. J. Cell Sci. 2003, 116:3453-3461.
44. Stapelbroek J.M., Peters T.A., van Beurden D.H., Curfs J.H., Joosten A., Beynon A.J., van Leeuwen B.M., van der Velden L.M., Bull L., Oude Elferink R.P., et al. ATP8B1 is essential for maintaining normal hearing. Proc. Natl. Acad. Sci. USA 2009, 106:9709-9714.
45. Gomes E., Jakobsen M.K., Axelsen K.B., Geisler M., Palmgren M.G. Chilling tolerance in Arabidopsis involves ALA1, a member of a new family of putative aminophospholipid translocases. Plant Cell 2000, 12:2441-2454.
46. Poulsen L.R., Lopez-Marques R.L., Palmgren M.G. Flippases: still more questions than answers. Cell Mol. Life Sci. 2008, 65:3119-3125.
47. Poulsen L.R., Lopez-Marques R.L., McDowell S.C., Okkeri J., Licht D., Schulz A., Pomorski T., Harper J.F., Palmgren M.G. The Arabidopsis P4-ATPase ALA3 localizes to the Golgi and requires a beta-subunit to function in lipid translocation and secretory vesicle formation. Plant Cell 2008, 20:658-676.
48. Chen C.Y., Ingram M.F., Rosal P.H., Graham T.R. Role for Drs2p, a P-type ATPase and potential aminophospholipid translocase, in yeast late Golgi function. J. Cell Biol. 1999, 147:1223-1236.
49. Lopez-Marques R.L., Poulsen L.R., Hanisch S., Meffert K., Buch-Pedersen M.J., Jakobsen M.K., Pomorski T.G., Palmgren M.G. Intracellular targeting signals and lipid specificity determinants of the ALA/ALIS P4-ATPase complex reside in the catalytic ALA {alpha}-subunit. Mol. Biol. Cell 2010.
50. Halleck M.S., Pradhan D., Blackman C., Berkes C., Williamson P., Schlegel R.A. Multiple members of a third subfamily of P-type ATPases identified by genomic sequences and ESTs. Genome Res. 1998, 8:354-361.
51. Ruaud A.F., Nilsson L., Richard F., Larsen M.K., Bessereau J.L., Tuck S. The C. elegans P4-ATPase TAT-1 regulates lysosome biogenesis and endocytosis. Traffic 2009, 10:88-100.
52. Zullig S., Neukomm L.J., Jovanovic M., Charette S.J., Lyssenko N.N., Halleck M.S., Reutelingsperger C.P., Schlegel R.A., Hengartner M.O. Aminophospholipid translocase TAT-1 promotes phosphatidylserine exposure during C. elegans apoptosis. Curr. Biol. 2007, 17:994-999.
53. Darland-Ransom M., Wang X., Sun C.L., Mapes J., Gengyo-Ando K., Mitani S., Xue D. Role of C. elegans TAT-1 protein in maintaining plasma membrane phosphatidylserine asymmetry. Science 2008, 320:528-531.
54. Seamen E., Blanchette J.M., Han M. P-type ATPase TAT-2 negatively regulates monomethyl branched-chain fatty acid mediated function in post-embryonic growth and development in C. elegans. PLoS Genet. 2009, 5:e1000589.
55. Lyssenko N.N., Miteva Y., Gilroy S., Hanna-Rose W., Schlegel R.A. An unexpectedly high degree of specialization and a widespread involvement in sterol metabolism among the C. elegans putative aminophospholipid translocases. BMC Dev. Biol. 2008, 8:96.
56. Harris M.J., Arias I.M. FIC1, a P-type ATPase linked to cholestatic liver disease, has homologues (ATP8B2 and ATP8B3) expressed throughout the body. Biochim. Biophys. Acta 2003, 1633:127-131.
57. Lein E.S., Hawrylycz M.J., Ao N., Ayres M., Bensinger A., Bernard A., Boe A.F., Boguski M.S., Brockway K.S., Byrnes E.J., et al. Genome-wide atlas of gene expression in the adult mouse brain. Nature 2007, 445:168-176.
58. Ding J., Wu Z., Crider B.P., Ma Y., Li X., Slaughter C., Gong L., Xie X.S. Identification and functional expression of four isoforms of ATPase II, the putative aminophospholipid translocase. Effect of isoform variation on the ATPase activity and phospholipid specificity. J. Biol. Chem. 2000, 275:23378-23386.
59. Paterson J.K., Renkema K., Burden L., Halleck M.S., Schlegel R.A., Williamson P., Daleke D.L. Lipid specific activation of the murine P4-ATPase Atp8a1 (ATPase II). Biochemistry 2006, 45:5367-5376.
60. Bull L.N., van Eijk M.J., Pawlikowska L., DeYoung J.A., Juijn J.A., Liao M., Klomp L.W., Lomri N., Berger R., Scharschmidt B.F., et al. A gene encoding a P-type ATPase mutated in two forms of hereditary cholestasis. Nat. Genet. 1998, 18:219-224.
61. van Mil S.W., Houwen R.H., Klomp L.W. Genetics of familial intrahepatic cholestasis syndromes. J. Med. Genet. 2005, 42:449-463.
62. Eppens E.F., van Mil S.W., de Vree J.M., Mok K.S., Juijn J.A., Oude Elferink R.P., Berger R., Houwen R.H., Klomp L.W. FIC1, the protein affected in two forms of hereditary cholestasis, is localized in the cholangiocyte and the canalicular membrane of the hepatocyte. J. Hepatol. 2001, 35:436-443.
63. van Mil S.W., van Oort M.M., van den Berg I., Berger R., Houwen R.H., Klomp L.W. Fic1 is expressed at apical membranes of different epithelial cells in the digestive tract and is induced in the small intestine during postnatal development of mice. Pediatr. Res. 2004, 56:981-987.
64. Pawlikowska L., Groen A., Eppens E.F., Kunne C., Ottenhoff R., Looije N., Knisely A.S., Killeen N.P., Bull L.N., Elferink R.P., et al. A mouse genetic model for familial cholestasis caused by ATP8B1 mutations reveals perturbed bile salt homeostasis but no impairment in bile secretion. Hum. Mol. Genet. 2004, 13:881-892.
65. Folmer D.E., van der Mark V.A., Ho-Mok K.S., Oude Elferink R.P., Paulusma C.C. Differential effects of progressive familial intrahepatic cholestasis type 1 and benign recurrent intrahepatic cholestasis type 1 mutations on canalicular localization of ATP8B1. Hepatology 2009.
66. van der Velden L.M., Stapelbroek J.M., Krieger E., van den Berghe P.V., Berger R., Verhulst P.M., Holthuis J.C., Houwen R.H., Klomp L.W., van de Graaf S.F. Folding defects in P-type ATP 8B1 associated with hereditary cholestasis are ameliorated by 4-phenylbutyrate. Hepatology 2009.
67. Paulusma C.C., de Waart D.R., Kunne C., Mok K.S., Elferink R.P. Activity of the bile salt export pump (ABCB11) is critically dependent on canalicular membrane cholesterol content. J. Biol. Chem. 2009, 284:9947-9954.
68. Groen A., Kunne C., Jongsma G., van den O.K., Mok K.S., Petruzzelli M., Vrins C.L., Bull L., Paulusma C.C., Oude Elferink R.P. Abcg5/8 independent biliary cholesterol excretion in Atp8b1-deficient mice. Gastroenterology 2008, 134:2091-2100.
69. Cai S.Y., Gautam S., Nguyen T., Soroka C.J., Rahner C., Boyer J.L. ATP8B1 deficiency disrupts the bile canalicular membrane bilayer structure in hepatocytes, but FXR expression and activity are maintained. Gastroenterology 2009, 136:1060-1069.
70. Paulusma C.C., Groen A., Kunne C., Ho-Mok K.S., Spijkerboer A.L., Rudi de W.D., Hoek F.J., Vreeling H., Hoeben K.A., Hoeben K.A., van M.J., et al. Atp8b1 deficiency in mice reduces resistance of the canalicular membrane to hydrophobic bile salts and impairs bile salt transport. Hepatology 2006, 44:195-204.
71. Oude Elferink R.P.J., Paulusma C.C., Groen A.K. Hepatocanalicular transport defects: pathophysiologic mechanisms of rare diseases. Gastroenterology 2006, 130:908-925.
72. Paulusma C.C., Folmer D.E., Ho-Mok K.S., de Waart D.R., Hilarius P.M., Verhoeven A.J., Oude Elferink R.P. ATP8B1 requires an accessory protein for endoplasmic reticulum exit and plasma membrane lipid flippase activity. Hepatology 2008, 47:268-278.
73. Bull L.N., Carlton V.E., Stricker N.L., Baharloo S., DeYoung J.A., Freimer N.B., Magid M.S., Kahn E., Markowitz J., DiCarlo F.J., et al. Genetic and morphological findings in progressive familial intrahepatic cholestasis (Byler disease [PFIC-1] and Byler syndrome): evidence for heterogeneity. Hepatology 1997, 26:155-164.
74. Wang L., Beserra C., Garbers D.L. A novel aminophospholipid transporter exclusively expressed in spermatozoa is required for membrane lipid asymmetry and normal fertilization. Dev. Biol. 2004, 267:203-215.
75. Gong E.Y., Park E., Lee H.J., Lee K. Expression of Atp8b3 in murine testis and its characterization as a testis specific P-type ATPase. Reproduction 2009, 137:345-351.
76. Xu P., Okkeri J., Hanisch S., Hu R.Y., Xu Q., Pomorski T.G., Ding X.Y. Identification of a novel mouse P4-ATPase family member highly expressed during spermatogenesis. J. Cell Sci. 2009, 122:2866-2876.
77. Dhar M.S., Yuan J.S., Elliott S.B., Sommardahl C. A type IV P-type ATPase affects insulin-mediated glucose uptake in adipose tissue and skeletal muscle in mice. J. Nutr. Biochem. 2006, 17:811-820.
78. Dhar M.S., Sommardahl C.S., Kirkland T., Nelson S., Donnell R., Johnson D.K., Castellani L.W. Mice heterozygous for Atp10c, a putative amphipath, represent a novel model of obesity and type 2 diabetes. J. Nutr. 2004, 134:799-805.
79. Flamant S., Pescher P., Lemercier B., Clement-Ziza M., Kepes F., Fellous M., Milon G., Marchal G., Besmond C. Characterization of a putative type IV aminophospholipid transporter P-type ATPase. Mamm. Genome 2003, 14:21-30.
80. Collins S., Martin T.L., Surwit R.S., Robidoux J. Genetic vulnerability to diet-induced obesity in the C57BL/6J mouse: physiological and molecular characteristics. Physiol. Behav. 2004, 81:243-248.
81. Li H., Wetten S., Li L., St Jean P.L., Upmanyu R., Surh L., Hosford D., Barnes M.R., Briley J.D., Borrie M., et al. Candidate single-nucleotide polymorphisms from a genomewide association study of Alzheimer disease. Arch. Neurol. 2008, 65:45-53.
82. Coleman J.A., Kwok M.C., Molday R.S. Localization, purification, and functional reconstitution of the P4-ATPase Atp8a2, a phosphatidylserine flippase in photoreceptor disc membranes. J. Biol. Chem. 2009, 284:32670-32679.
83. Kato U., Emoto K., Fredriksson C., Nakamura H., Ohta A., Kobayashi T., Murakami-Murofushi K., Kobayashi T., Umeda M. A novel membrane protein, Ros3p, is required for phospholipid translocation across the plasma membrane in Saccharomyces cerevisiae. J. Biol. Chem. 2002, 277:37855-37862.
84. Katoh Y., Katoh M. Identification and characterization of CDC50A, CDC50B and CDC50C genes in silico. Oncol. Rep. 2004, 12:939-943.
85. Perez-Victoria F.J., Sanchez-Canete M.P., Castanys S., Gamarro F. Phospholipid translocation and miltefosine potency require both L. donovani miltefosine transporter and the new protein LdRos3 in Leishmania parasites. J. Biol. Chem. 2006, 281:23766-23775.
86. Graham T.R. Flippases and vesicle-mediated protein transport. Trends Cell Biol. 2004, 14:670-677.
87. Puts C.F., Holthuis J.C. Mechanism and significance of P4 ATPase-catalyzed lipid transport: lessons from a Na+/K+-pump. Biochim. Biophys. Acta 2009, 1791:603-611.
88. Saito K., Fujimura-Kamada K., Furuta N., Kato U., Umeda M., Tanaka K. Cdc50p, a protein required for polarized growth, associates with the Drs2p P-type ATPase implicated in phospholipid translocation in Saccharomyces cerevisiae. Mol. Biol. Cell 2004, 15:3418-3432.
89. Geering K. The functional role of beta subunits in oligomeric P-type ATPases. J. Bioenerg. Biomembr. 2001, 33:425-438.
90. Blanco G. Na, K-ATPase subunit heterogeneity as a mechanism for tissue-specific ion regulation. Semin. Nephrol. 2005, 25:292-303.
91. Geering K. Functional roles of Na, K-ATPase subunits. Curr. Opin. Nephrol. Hypertens. 2008, 17:526-532.
92. Muth T.R., Gottardi C.J., Roush D.L., Caplan M.J. A basolateral sorting signal is encoded in the alpha-subunit of Na-K-ATPase. Am. J. Physiol. 1998, 274:C688-C696.
93. Vagin O., Turdikulova S., Sachs G. The H, K-ATPase beta subunit as a model to study the role of N-glycosylation in membrane trafficking and apical sorting. J. Biol. Chem. 2004, 279:39026-39034.
94. Caplan M.J. Ion pumps in epithelial cells: sorting, stabilization, and polarity. Am. J. Physiol. 1997, 272:G1304-G1313.
95. Ruiz A., Bhat S.P., Bok D. Expression and synthesis of the Na, K-ATPase beta 2 subunit in human retinal pigment epithelium. Gene 1996, 176:237-242.
96. Mobasheri A., Oukrif D., Dawodu S.P., Sinha M., Greenwell P., Stewart D., Djamgoz M.B., Foster C.S., Martin-Vasallo P., Mobasheri R. Isoforms of Na+, K+-ATPase in human prostate; specificity of expression and apical membrane polarization. Histol. Histopathol. 2001, 16:141-154.
97. Ernst S.A., Palacios J.R., Siegel G.J. Immunocytochemical localization of Na+, K+-ATPase catalytic polypeptide in mouse choroid plexus. J. Histochem. Cytochem. 1986, 34:189-195.
98. Wilson P.D., Devuyst O., Li X., Gatti L., Falkenstein D., Robinson S., Fambrough D., Burrow C.R. Apical plasma membrane mispolarization of NaK-ATPase in polycystic kidney disease epithelia is associated with aberrant expression of the beta2 isoform. Am. J. Pathol. 2000, 156:253-268.
99. Vagin O., Turdikulova S., Sachs G. Recombinant addition of N-glycosylation sites to the basolateral Na, K-ATPase beta1 subunit results in its clustering in caveolae and apical sorting in HGT-1 cells. J. Biol. Chem. 2005, 280:43159-43167.
100. Hanson P.K., Malone L., Birchmore J.L., Nichols J.W. Lem3p is essential for the uptake and potency of alkylphosphocholine drugs, edelfosine and miltefosine. J. Biol. Chem. 2003, 278:36041-36050.
101. Noji T., Yamamoto T., Saito K., Fujimura-Kamada K., Kondo S., Tanaka K. Mutational analysis of the Lem3p-Dnf1p putative phospholipid-translocating P-type ATPase reveals novel regulatory roles for Lem3p and a carboxyl-terminal region of Dnf1p independent of the phospholipid-translocating activity of Dnf1p in yeast. Biochem. Biophys. Res. Commun. 2006, 344:323-331.
102. Osada N., Hashimoto K., Hirai M., Kusuda J. Aberrant termination of reproduction-related TMEM30C transcripts in the hominoids. Gene 2007, 392:151-156.
103. Xu P., Ding X. Characterization and expression of mouse Cdc50c during spermatogenesis. Acta Biochim. Biophys. Sin. (Shanghai) 2007, 39:739-744.
104. Lenoir G., Williamson P., Puts C.F., Holthuis J.C. Cdc50p plays a vital role in the ATPase reaction cycle of the putative aminophospholipid transporter drs2p. J. Biol. Chem. 2009, 284:17956-17967.
105. Kwok M.C., Holopainen J.M., Molday L.L., Foster L.J., Molday R.S. Proteomics of photoreceptor outer segments identifies a subset of SNARE and Rab proteins implicated in membrane vesicle trafficking and fusion. Mol. Cell Proteomics 2008, 7:1053-1066.
106. Sheetz M.P., Singer S.J. Biological membranes as bilayer couples. A molecular mechanism of drug-erythrocyte interactions. Proc. Natl. Acad. Sci. USA 1974, 71:4457-4461.
107. Farge E., Ojcius D.M., Subtil A., Dautry-Varsat A. Enhancement of endocytosis due to aminophospholipid transport across the plasma membrane of living cells. Am. J. Physiol. 1999, 276:C725-C733.
108. Pomorski T., Holthuis J.C., Herrmann A., van Meer G. Tracking down lipid flippases and their biological functions. J. Cell Sci. 2004, 117:805-813.
109. Saito K., Fujimura-Kamada K., Hanamatsu H., Kato U., Umeda M., Kozminski K.G., Tanaka K. Transbilayer phospholipid flipping regulates Cdc42p signaling during polarized cell growth via Rga GTPase-activating proteins. Dev. Cell 2007, 13:743-751.
110. Halleck M.S., Schlegel R.A., Williamson P.L. Reanalysis of ATP11B, a type IV P-type ATPase. J. Biol. Chem. 2002, 277:9736-9740.